Trophic Groups of Demersal Fish of Santos Bay and Adjacent Continental Shelf, São Paulo State, Brazil: Temporal and Spatial Comparisons
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BRAZILIAN JOURNAL OF OCEANOGRAPHY, 62(2):89-102, 2014 TROPHIC GROUPS OF DEMERSAL FISH OF SANTOS BAY AND ADJACENT CONTINENTAL SHELF, SÃO PAULO STATE, BRAZIL: TEMPORAL AND SPATIAL COMPARISONS Elizabeti Y. Muto1,*, Thaïs Navajas Corbisier1, Leandro Inoe Coelho1, Lidia Paes Leme Arantes1, André Chalom2 and Lucy Satiko Hashimoto Soares1 1Instituto Oceanográfico da Universidade de São Paulo (Praça do Oceanográfico, 191, 05508-120 São Paulo, SP, Brasil) 2Instituto de Matemática e Estatística da Universidade de São Paulo (Rua do Matão 1010, 05508-050 São Paulo, SP, Brasil) *Corresponding author: [email protected] http://dx.doi.org/10.1590/S1679-87592014045906202 A B S T R A C T The temporal and spatial variations of feeding habits and trophic groups of demersal fish species of Santos Bay and the adjacent continental shelf were investigated. The samples were taken in September 2005 and March 2006 by bottom otter trawling. The stomach content analysis of 2,328 specimens of 49 species showed most fish fed on a large range of food items but relied heavily on shrimp, crabs/swimming-crabs, amphipods, mysids, polychaetes, ophiuroids, squids, and teleosteans. The species were classified into ten trophic groups. Shrimp were an important food source in the Santos bay and inner shelf, while ophiuroids were important prey for predators of the middle shelf. Many species relied on crabs/swimming-crabs during the summer, especially on the middle shelf. The spatial and temporal variability in food resource utilization by fish were related to the pattern of distribution and abundance of their prey. The predation on shrimp and crabs/swimming-crabs seems to be related to the water mass dynamics of the region. Intraspecific comparisons demonstrated that most of the species display spatial and/or temporal variation in their diet. The demersal ichtyofauna can also be divided into the more general categories of piscivores, nektonic invertebrate feeders, benthic invertebrate feeders and planktonic invertebrate feeders. R E S U M O A variação temporal e espacial dos hábitos alimentares e dos grupos tróficos de peixes demersais abundantes na baía de Santos e plataforma continental adjacente foi investigada. As amostras foram obtidas em setembro de 2005 e março de 2006, utilizando-se rede de arrasto de fundo. A análise dos conteúdos estomacais de 2.328 exemplares de 49 espécies demonstrou que a maioria se alimentou de uma grande variedade de presas, destacando-se os camarões, caranguejos/siris, anfípodes, misidáceos, poliquetas, ofiuróides, lulas e teleósteos. De acordo com as presas principais, os peixes foram agrupados em dez grupos tróficos. Os camarões foram presas importantes na baía e plataforma interna, e os ofiuróides apenas na plataforma média. Caranguejos/siris tiveram grande importância na dieta de várias espécies durante o verão, em especial na plataforma média. A variação espacial e temporal na alimentação dos peixes esteve associada ao padrão de distribuição e abundância de suas presas. A ingestão de camarões e caranguejos/siris está, provavelmente, associada à dinâmica das massas de água na região. Comparações intraespecíficas demonstraram que a maioria das espécies apresenta variação espacial e/ou temporal na dieta. A ictiofauna demersal pode ser categorizada em grupos tróficos mais abrangentes: piscívoros, comedores de invertebrados nectônicos, comedores de invertebrados bentônicos e comedores de invertebrados planctônicos. Descriptors: Diet, Stomach content, Marine fish, Teleostei, Elasmobranchii, Southeastern Brazil. Descritores: Dieta, Conteúdos estomacais, Peixes marinhos, Teleostei, Elasmobranchii, Sudeste do Brasil. INTRODUCTION (419,400 inhab.) and São Vicente (332,445 inhab.) being the most heavily populated (IBGE, 2010). It The Baixada Santista is the main tourist constitutes a complex ecosystem with brackish and coastal area of São Paulo State; its metropolitan region marine waters, islands, internal channels, estuaries, encompasses nine municipalities, with Santos mangrove forests, and rainforest. Monitored by the 90 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 62(2), 2014 State Environmental Agency (CETESB) since 1980, mentioning (SOARES et al., 1992; SOARES et al., part of its marine zone was officially proclaimed as a 1993; PIRES-VANIN et al., 1993; SOARES et al., Conservation Unit of Sustainable Use (SÃO PAULO, 2008). 2008a). It is an area subject to great environmental The present study was carried out in support impacts, with many sources of anthropogenic of the project ECOSAN-subproject Trophodynamics, pollution. The sewage disposal from the Santos and which assessed the food web of the Santos region São Vicente estuaries promotes the eutrophication of using stable isotopes (SI) of carbon (δ13C) and Santos Bay and neighboring coastal waters, mainly nitrogen (δ15N). While stable isotopes (SI) indicate the during the summer. In addition to the port of Santos main sources of energy for consumers based on the (the most important in Brazil), the industrial complex assimilated food (PETERSON; FRY, 1987), stomach of Cubatão is responsible for the great volume of content data provide the taxonomic status of the prey industrial effluents in the coastal region. ingested, and together with natural history information Marine and estuarine fisheries are an provide additional insights to support SI conclusions important economic activity; the landings in Santos (PETERSON, 1999). We selected dominant species in were responsible for ~60% of the total catch of São the region as well as those representing important food Paulo State in 2010 (22,094.6 t) and 2011 (20,931.9 t) habits. The species surveyed made up 92% and 85% (INSTITUTO DE PESCA, 2011, 2012). The sciaenids of the abundance in Santos Bay (DIAS, J.F., pers. are the main target of the regional fishery, especially comm.) and continental shelf (DIAS et al., 2008), the white mouth, Micropogonias furnieri; the Jamaica respectively. Of the 49 species analyzed, 8.2% are weakfish, Cynoscion jamaicensis; and the king threatened with extinction (Atlantoraja cyclophora, weakfish, Macrodon atricauda (VALENTINNI et al., Urophycis brasiliensis, Cynoscion jamaicensis, and 1991; ÁVILA-DA-SILVA et al., 2005). Paralichthys patagonicus) and 14.3% (Lophius Information on the diversity and temporal gastrophysus, Merluccius hubbsi, Macrodon and spatial variation of the demersal ichthyofauna are atricauda, Micropogonias furnieri, Umbrina canosai, available for the continental shelf located to the north and two elasmobranchs - Rioraja agassizii and of the area studied (ROSSI-WONGTSCHOWSKI; Rhinobatos percelens) are overexploited in São Paulo PAES, 1993; ROCHA; ROSSI-WONGTSCHOWSKI, State (SÃO PAULO, 2008b). Therefore, 1998; MUTO et al., 2000). However, there are fewer understanding the biology of these species and their data for the present study site. The estuarine complex role in the ecosystem is critical for monitoring of Santos-São Vicente represents one of the most programs. Specifically, this study sought to identify important nursery grounds for the ichthyofauna, the diet of dominant fish species of Santos Bay and the characterized by high fish diversity and abundance continental shelf and the trophic structure of the fish (PAIVA FILHO et al., 1987). The sciaenid fish are the assemblage. The temporal and spatial variability of the most abundant family in Santos Bay all year round trophic groups were also assessed. (GIANNINI; PAIVA FILHO, 1990). Human activities influence fish diversity and promote changes in the MATERIAL AND METHODS trophic interactions. For example, the replacement of long-lived piscivore fish by small planktivore fish and Sampling invertebrates in the overall fishery landings indicates the impact of fishing on the structure of marine food The samples were collected during two webs, affecting the abundance of top predators and research cruises conducted from 9 to 15 September promoting long-term changes in the number of species (late austral winter, W) and 1 to 6 March 2006 (late (PAULY et al., 1998; PAULY; WATSON, 2005). austral summer, S) on board the Research Vessel Prof. Identification of food web linkages is a W. Besnard (Oceanographic Institute, University of major goal in ecology because it provides basic São Paulo) within the scope of the project “The information on trophic flows and the potential for Influence of the estuarine complex of the Baixada interspecific interactions (REUM; ESSINGTON, Santista on the adjacent continental shelf''s ecosystem 2008). Dietary data are essential to trace these (ECOSAN) - subproject Trophodynamics”. Fish were linkages, enabling managers to cope with complex collected using a bottom otter trawl with a 17-m net issues, such as biological control, conservation, and (60-mm stretch-mesh in the body and sleeve and 25 fishery management. Many studies have been mm at the cod end), and frozen at -20ºC. Fifteen and conducted to clarify the trophic relationships of the thirty-minute hauls at the speed of 2 knots were coastal fish of Southeastern Brazil; however, the carried out in Santos Bay and on the continental shelf, comprehensive studies carried out for the demersal respectively. The fishing was conducted in two fish assemblage off Ubatuba and São Sebastião shelf areas of Santos Bay (A1, A2; depth = 8.9 to 11 m) (north coast of São Paulo) showing the main energy and six areas on the continental shelf, four of them pathway supporting fish production are worth located on the inner shelf (IS: A3, A4, A7, P9; depth = MUTO ET AL.: TROPHIC GROUPS OF DEMERSAL